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.2002 May 28;99(11):7687-92.
doi: 10.1073/pnas.122108599.

The evolutionary history of methicillin-resistant Staphylococcus aureus (MRSA)

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The evolutionary history of methicillin-resistant Staphylococcus aureus (MRSA)

Mark C Enright et al. Proc Natl Acad Sci U S A..

Abstract

Methicillin-resistant Staphylococcus aureus (MRSA) is a major cause of hospital-acquired infections that are becoming increasingly difficult to combat because of emerging resistance to all current antibiotic classes. The evolutionary origins of MRSA are poorly understood, no rational nomenclature exists, and there is no consensus on the number of major MRSA clones or the relatedness of clones described from different countries. We resolve all of these issues and provide a more thorough and precise analysis of the evolution of MRSA clones than has previously been possible. Using multilocus sequence typing and an algorithm, BURST, we analyzed an international collection of 912 MRSA and methicillin-susceptible S. aureus (MSSA) isolates. We identified 11 major MRSA clones within five groups of related genotypes. The putative ancestral genotype of each group and the most parsimonious patterns of descent of isolates from each ancestor were inferred by using BURST, which, together with analysis of the methicillin resistance genes, established the likely evolutionary origins of each major MRSA clone, the genotype of the original MRSA clone and its MSSA progenitor, and the extent of acquisition and horizontal movement of the methicillin resistance genes. Major MRSA clones have arisen repeatedly from successful epidemic MSSA strains, and isolates with decreased susceptibility to vancomycin, the antibiotic of last resort, are arising from some of these major MRSA clones, highlighting a depressing progression of increasing drug resistance within a small number of ecologically successful S. aureus genotypes.

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Figures

Figure 1
Figure 1
Relatedness of MRSA isolates. The 359 MRSA isolates were resolved by MLST into 38 STs, and a dendrogram was constructed from the pairwise differences in their allelic profiles. * identifies a major cluster of related STs, which includes four of the major EMRSA STs (and five of the major EMRSA clones) and all but one of the MRSA isolates from the 1960s. ● denote the seven major international EMRSA STs and one additional EMRSA ST (ST36) that was very abundant in the dataset, but that was largely restricted to the United Kingdom (Table 1).
Figure 2
Figure 2
Analysis ofS. aureus isolates withburst. The collection of 914S. aureus isolates was analyzed byburst, and the five CCs that included MRSA isolates are shown. CCs are named after the ST predicted to be the ancestral genotype (e.g., CC8). The ST prefix is not shown (i.e., 250 corresponds to ST250). The ST of the predicted ancestral genotype is placed in the central circle, SLVs are within the second circle, and double locus variants within the outer dotted circle. Three isolates within CCs but that are not SLVs or double locus variants of the ancestral genotype are also shown (STs 222, 312, and 518). One further small group of isolates for which an ancestral genotype cannot be inferred and three STs that are not members of any CC (singletons) are also shown. The major EMRSA STs are underlined. MRSA STs are shown in red, MSSA STs in blue, and GISA STs in green. In some cases the same ST includes MRSA and MSSA isolates and, for ST5, also GISA isolates. Some MRSA STs include more than one MRSA clone, identified by the presence of different SCCmec types (Table 1). Where more than one, the number of isolates in each ST is shown in parentheses.
Figure 3
Figure 3
Evolutionary origins and patterns of descent within CC8. ST8 is the predicted ancestor of the CC8 CC. Alterations in the allelic profile (and the locus that has changed), and the acquisition of the SCCmec types are shown. The five major EMRSA clones are underlined. All except one of the MRSA isolates from the 1960s are within the STs included in the box. For isolates outside the box not all SLVs are shown. ST250–MSSA isolates were not present in our collection but have been described (26).
Figure 4
Figure 4
Evolutionary origins and patterns of descent within CC5 and CC30. (A) The proposed pathways to the major EMRSA clones of ST5 (underlined) and the origins of GISA–ST5-II are shown. (B) The origin of MRSA–ST36-II (underlined) is shown. MSSA–ST36 is on the proposed evolutionary pathway from MSSA–ST30 to MRSA–ST36 but isolates with this genotype have not been observed so far. Other details are as in Fig. 3. Not all SLVs are shown.
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